New hallmarks of criticality in recurrent neural networks

A rigorous understanding of brain dynamics and function requires a conceptual bridge between multiple levels of organization, including neural spiking and network-level population activity. Mounting evidence suggests that neural networks of cerebral cortex operate at criticality. How operating near this network state impacts the variability of neuronal spiking is largely unknown. Here we show in a computational model that two prevalent features of cortical single-neuron activity, irregular spiking and the decline of response variability at stimulus onset, are both emergent properties of a recurrent network operating near criticality. Importantly, our work reveals that the relation between the irregularity of spiking and the number of input connections to a neuron, i.e., the in-degree, is maximized at criticality. Our findings establish criticality as a unifying principle for the variability of single-neuron spiking and the collective behavior of recurrent circuits in cerebral cortex.

[1]  Tang,et al.  Self-Organized Criticality: An Explanation of 1/f Noise , 2011 .

[2]  A. Litwin-Kumar,et al.  Slow dynamics and high variability in balanced cortical networks with clustered connections , 2012, Nature Neuroscience.

[3]  W. Newsome,et al.  The Variable Discharge of Cortical Neurons: Implications for Connectivity, Computation, and Information Coding , 1998, The Journal of Neuroscience.

[4]  Woodrow L. Shew,et al.  Adaptation to sensory input tunes visual cortex to criticality , 2015, Nature Physics.

[5]  Wulfram Gerstner,et al.  Neuronal Dynamics: From Single Neurons To Networks And Models Of Cognition , 2014 .

[6]  William R. Softky,et al.  The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  Haim Sompolinsky,et al.  Stimulus-dependent suppression of intrinsic variability in recurrent neural networks , 2010, BMC Neuroscience.

[8]  Narayan Srinivasa,et al.  Synaptic Plasticity Enables Adaptive Self-Tuning Critical Networks , 2015, PLoS Comput. Biol..

[9]  John M. Beggs,et al.  Neuronal Avalanches in Neocortical Circuits , 2003, The Journal of Neuroscience.

[10]  Christian K. Machens,et al.  Efficient codes and balanced networks , 2016, Nature Neuroscience.

[11]  Dan-Mei Chen,et al.  Self-organized criticality in a cellular automaton model of pulse-coupled integrate-and-fire neurons , 1995 .

[12]  Haim Sompolinsky,et al.  Computational neuroscience: beyond the local circuit , 2014, Current Opinion in Neurobiology.

[13]  Andrew M. Clark,et al.  Stimulus onset quenches neural variability: a widespread cortical phenomenon , 2010, Nature Neuroscience.

[14]  Oren Shriki,et al.  Near-Critical Dynamics in Stimulus-Evoked Activity of the Human Brain and Its Relation to Spontaneous Resting-State Activity , 2015, The Journal of Neuroscience.

[15]  Nicholas A. Steinmetz,et al.  Diverse coupling of neurons to populations in sensory cortex , 2015, Nature.

[16]  L. F. Abbott,et al.  Generating Coherent Patterns of Activity from Chaotic Neural Networks , 2009, Neuron.

[17]  E. Ott,et al.  Statistical properties of avalanches in networks. , 2012, Physical review. E, Statistical, nonlinear, and soft matter physics.

[18]  Stefan Mihalas,et al.  Self-organized criticality occurs in non-conservative neuronal networks during Up states , 2010, Nature physics.

[19]  Srdjan Ostojic,et al.  Two types of asynchronous activity in networks of excitatory and inhibitory spiking neurons , 2014, Nature Neuroscience.

[20]  Marc Benayoun,et al.  Avalanches in a Stochastic Model of Spiking Neurons , 2010, PLoS Comput. Biol..

[21]  Andreas Klaus,et al.  Irregular spiking of pyramidal neurons organizes as scale-invariant neuronal avalanches in the awake state , 2015, eLife.

[22]  John M. Beggs,et al.  Being Critical of Criticality in the Brain , 2012, Front. Physio..

[23]  J. M. Herrmann,et al.  Finite-size effects of avalanche dynamics. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[24]  H. Sompolinsky,et al.  Chaos in Neuronal Networks with Balanced Excitatory and Inhibitory Activity , 1996, Science.

[25]  A. Aertsen,et al.  Conditions for Propagating Synchronous Spiking and Asynchronous Firing Rates in a Cortical Network Model , 2008, The Journal of Neuroscience.

[26]  L. Abbott,et al.  Stimulus-dependent suppression of chaos in recurrent neural networks. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

[27]  C. Stevens,et al.  Input synchrony and the irregular firing of cortical neurons , 1998, Nature Neuroscience.

[28]  Woodrow L. Shew,et al.  Predicting criticality and dynamic range in complex networks: effects of topology. , 2010, Physical review letters.

[29]  D. Plenz,et al.  Criticality in neural systems , 2014 .